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Antibiotic Activity Altered by Competitive Interactions Between Two Coral Reef–Associated Bacteria

  • Microbiology of Aquatic Systems
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Abstract

Microbes produce natural products that mediate interactions with each other and with their environments, representing a potential source of antibiotics for human use. The biosynthesis of some antibiotics whose constitutive production otherwise remains low has been shown to be induced by competing microbes. Competition among macroorganism hosts may further influence the metabolic outputs of members of their microbiomes, especially near host surfaces where hosts and microbial symbionts come into close contact. At multiple field sites in Fiji, we collected matched samples of corals and algae that were freestanding or in physical contact with each other, cultivated bacteria from their surfaces, and explored growth-inhibitory activities of these bacteria against marine and human pathogens. In the course of the investigation, an interaction was discovered between two coral-associated actinomycetes in which an Agrococcus sp. interfered with the antibiotic output of a Streptomyces sp. Several diketopiperazines identified from the antibiotic-producing bacterium could not, on their own, account for the antibiotic activity indicating that other, as yet unidentified molecule(s) or molecular blends, possibly including diketopiperazines, are likely involved. This observation highlights the complex molecular dynamics at play among microbiome constituents. The mechanisms through which microbial interactions impact the biological activities of specialized metabolites deserve further attention considering the ecological and commercial importance of bacterial natural products.

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Data Availability

16S sequences for the microbes used in this study have been deposited in GenBank (OK184772-OK184808). All other data generated or analyzed during this study are included in this published article (and its supplementary information files) unless otherwise noted. Microbial isolates are stored at the Georgia Institute of Technology and are available upon request.

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Not applicable.

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Acknowledgements

We thank the Fijian Government for the permission to perform research in their territorial waters and for permission to export samples. We also thank the chief, Ratu Manasa Naikasowalu, and the village of Nacula, as well as the staff at the Oarsman Bay Lodge, for their support in making this collection expedition possible. Analytical support was provided by the Georgia Institute of Technology NMR Center and the Georgia Institute of Technology Bioanalytical Mass Spectrometry Facility. Vibrio coralliilyticus CN2 was provided by Dr. Mark Hay at the Georgia Institute of Technology.

Funding

The project was funded by NIH U19 TW007401.

Author information

Authors and Affiliations

  1. Institute for Bioengineering and Bioscience, Center for Microbial Dynamics and Infection, School of Biological Sciences and School of Chemistry & Biochemistry, Georgia Institute of Technology, Atlanta, GA, USA

    Samantha J. Mascuch & Julia Kubanek

  2. Center for Marine Biotechnology and Biomedicine, Scripps Institution of Oceanography, UC San Diego, La Jolla, CA, USA

    Alyssa Demko & Paul Jensen

  3. School of Biological and Chemical Sciences, The University of the South Pacific, Suva, Fiji

    Samson Viulu, Joape Ginigini & Katy Soapi

Authors
  1. Samantha J. Mascuch
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  2. Alyssa Demko
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  3. Samson Viulu
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  4. Joape Ginigini
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  5. Katy Soapi
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  6. Paul Jensen
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  7. Julia Kubanek
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Contributions

SJM, PJ, and JK conceived of and designed experiments. SJM, AD, SV, JG, KS, PJ, and JK contributed to fieldwork, microbial isolation efforts, and subsequent experiments. The manuscript was written by SJM and JK with input from all authors.

Corresponding author

Correspondence to Julia Kubanek.

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Ethics Approval

The research conducted here complied with the Convention on the Trade in Endangered Species of Wild Fauna and Flora (CITES permit #17FJ/NV2000284) and abided by the legal agreement between the Georgia Institute of Technology, Scripps Institution of Oceanography, The University of the South Pacific, and the Fijian Government.

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All authors have reviewed the manuscript and consent to its publication.

Conflict of Interest

The authors declare no competing interests.

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Mascuch, S.J., Demko, A., Viulu, S. et al. Antibiotic Activity Altered by Competitive Interactions Between Two Coral Reef–Associated Bacteria. Microb Ecol 85, 1226–1235 (2023). https://doi.org/10.1007/s00248-022-02016-6

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  • DOI: https://doi.org/10.1007/s00248-022-02016-6

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